AN INTERAURAL ELECTRODE PAIRING CLINICAL RESEARCH SYSTEM FORBILATERAL COCHLEAR IMPLANTS

Hongmei Hu, Stephan Ewert, Tom Campbell, Birger Kollmeier, Mathias Dietz

Medizinische Physik, Universitat Oldenburg and Cluster of Excellence “Hearing4all”, Germany

ABSTRACT

Bilateral cochlear implants (BiCIs) have succeeded in improv-

ing the spatial hearing performance of bilateral CI users, albeit with

considerable variability across implantees. Limited success can be

caused by an interaural mismatch of the place-of-stimulation that

arises from electrode arrays being inserted at different depths in

each cochlea. In comparison to subjective pairing methods such as

pitch matching, one promising objective measure based on electri-

cally evoked auditory brainstem responses (EABR), the binaural in-

teraction component (BIC), could be used to optimize the interaural

electrode pairing (IEP) in BiCIs. Matched interaural electrodes are

expected to facilitate binaural functions such as binaural fusion, lo-

calization, or detection of signals in noise. An IEP system, currently

under development for clinical research, is proposed. The system of-

fers subjective and objective IEP methods for BiCI: a psychoacous-

tic test module for pitch ranking and interaural pulse time difference

(IPTD) sensitivity, and a binaural and monaural EABR recording

module to derive the BIC. Psychoacoustic and IEP measures from

two implantees are presented.

Index Terms— Bilateral cochlear implants, EEG, Binaural in-

teraction components, Interaural electrode pairing, Objective mea-

sures

1. INTRODUCTION

Bilateral cochlear implantation has sought to restore the advantages

of binaural hearing to the deaf by providing binaural cues normally

important for binaural perception. Most bilateral cochlear implant

(BiCI) users have shown improvements in sound localization com-

pared to their ability when using only one CI. However, compared to

normal hearing (NH) individuals, localization accuracy of BiCI users

has still been much worse and there has remained a large variabili-

ty in performance amongst CI users [1–4]. One reason identified for

the difference in performance between CI and NH subjects is that the

inputs to the NH binaural system from the two ears can be assumed

to be well matched, whilst in CI users the peripheral auditory inputs

to the binaural system at the two ears require appropriate matching

strategies, e.g. for interaural electrodes.

Several approaches have been used to define the best-matched

interaural electrode pairs for enabling binaural function for bilateral

CI users so that binaural fusion, localization and detection of signals

in noise could be maximized. The approaches include the clinical-

ly used computed tomography scans that match electrodes based on

insertion depth [5–7] and interaural pitch comparisons to aid inter-

aural electrode pairing [8–15]). Electrically evoked auditory brain-

This work was funded by European Union under the Advancing BinauralCochlear Implant Technology (ABCIT) grant agreement (No. 304912). Theauthors would like to thank Stefan Strahl (MED-EL) for RIB II support andthe participating CI users. (e-mail: hongmei.hu@uni-oldenburg.de).

stem response (EABR) measurements have emerged as a promising

method for assigning best-matched interaural electrode pairs. EABR

could potentially replace psychophysical approaches, especially for

pediatric patients. The hypothesis has been that, when two implants

are put into place, interaurally corresponding electrodes stimulate

auditory-nerve fibers from comparable cochlear regions in the two

ears. Accordingly, stimulation of such comparable pairs of elec-

trodes would cause an enhanced binaural interaction relative to s-

timulation of non-comparable pairs [16, 17]. He et al. corroborated

this hypothesis in CI users [13], demonstrating that the binaural in-

teraction component (BIC) of the EABR could be used to match

electrodes in bilateral CI users.

The aim of the current study was to establish a clinical research

system including subjective psychophysical listening tests and ob-

jective EABR recordings, to support an optimal interaural electrode

pairing (IEP) strategy in bilateral CI users. The IEP experiment

system was developed in MATLAB (Mathworks) for fast psychoa-

coustic testing and EABR recording. The system includes psychoa-

coustic pre-testing modules (e.g. loudness balancing), a pitch rank-

ing module, an interaural pulse time difference (IPTD) sensitivity-

testing module, and a binaural and monaural EABR module.

The paper is organized as follows: after introduction of the BIC

in BiCI users in Section 2, the IEP experiment system is described in

Section 3. The results from two BiCI adults are presented in Section

4, followed by the conclusion in Section 5.

2. BIC IN BILATERAL COCHLEAR IMPLANTEES

Binaural interaction has been demonstrated to occur in the subcor-

tical auditory system within the dorsal cochlear nucleus, superior

olivary nucleus, dorsal nucleus of the lateral nucleus, and the infe-

rior colliculus [18]. In evoked response studies, binaural processing

is assessed by the binaural interaction component. The BIC can be

isolated from the auditory brainstem response (ABR), an evoked re-

sponse in the electroencephalogram (EEG) that is generated by sub-

cortical structures. The BIC is defined as the difference between the

potential obtained with binaural stimulation (B) and the sum of the

potentials obtained with monaural stimulation (L+R), symbolically

BIC = B - (L+R) [19]. Any significant deviation from BIC = 0 is

understood to indicate a non-linear additivity, i.e. a functional cou-

pling of left and right signals. During the past 40 years, acoustically

stimulated BIC has been extensively investigated [19–21].

More recently, electrophysiological evidence of binaural inter-

action has also been revealed in bilateral CI users [13,17,22]. These

responses evoked by direct stimulation of cochlear-implant elec-

trodes rather than acoustical stimulation have been termed EABR,

and exhibit distinguishing characteristics from ABRs [18,21], name-

ly earlier peak latencies and higher peak amplitudes [23–25]. A

pronounced electrically evoked BIC, consisting of a negative peak

around 3.6 ms followed by a positive peak near 4.4 ms was shown

66978-1-4799-5403-2/14/$31.00 ©2014 IEEE ChinaSIP 2014

RIB II Detector box

Oscilloscope

RIB II

Cz

FPz

A1 A2

M1 M2

Oz

Headbox

Stimuli Check

EEG amplifier EEG

Recording

Computer

Trigger

Trigger

Computer

with NI I/O

Card

Electrically and acoustically shielded room Recording and observation room

To BiCIs

To Calibration

Fig. 1. The IEP clinical research system consists of sub-systems for

CI stimulation, and EEG recording. The upper part is calibration

in [16], being attributable to the fact that electrical pulses stimu-

lated fibers of the auditory nerve synchronously. Accordingly, the

established nature of the BIC, together with the high amplitude of

the electrically evoked BIC motivates a further investigation of the

electrically evoked BIC as a method for pairing the positions of

intracochlear electrodes [13, 16].

3. INTERAURAL ELECTRODE PAIRING CLINICAL

RESEARCH SYSTEM

The proposed IEP clinical research system is comprised of psy-

chophysical test procedures and an EEG procedure. Five monaural

and binaural (bilateral) psychophysical test procedures are included:

loudness estimation, loudness balancing, interaural pitch ranking,

sound image centering and IPTD sensitivity. The loudness estima-

tion procedure estimates the maximum comfortable level (MCL)

and hearing threshold (HL); the loudness balancing procedure de-

termines levels of equal loudness for each electrode pair; the pitch

ranking procedure identifies the pitch-matched electrodes; the sound

image centering is a pre-test and interaural level calibration for the

IPTD sensitivity procedure; and the IPTD procedure determines the

binaurally most sensitive electrode pair. EEG recordings then derive

scalp-measured EABRs, with the presentation level obtained from

the loudness balancing procedure. The IEP obtained by pitch rank-

ing and the IEP derived from the BIC tuning can then be compared

against the IEP drawn from IPTD sensitivity, which is defined as the

standard reference.

3.1. Equipment and stimuli

The stimulation and EEG setup for the current BiCIs IEP clinical

research system is schematized in Fig. 1. A research interface box

(RIB II, manufactured at University of Innsbruck, Austria) delivers

monaural or bilaterally synchronized electrical pulses directly to the

MED-EL CIs. Prior to the experiment, the stimuli are verified using

a detector box (a MED-EL CI simulator). A user-friendly graphical

user interface (GUI) as shown in Fig. 2 (a), controls the electri-

cal stimulation of the IEP clinical research system via a stimulation

computer with a National Instruments I/O card.

Most of the psychophysical tests are based on standardized pro-

cedures employed in previous BiCI studies [13, 17, 22, 26]. For

(a)

(b)

Fig. 2. The IEP CI experiment GUI is shown in panel (a), with

participant information to be entered on the left, and experiment se-

lection on the right. The experiment selection invokes the AFC and

EABR recording modules as indicated by the schematic outline of

the software in panel (b).

the psychophysical testing the freely available Oldenburg AFC soft-

ware [27] which was extended here to operate the RIB II interface, is

invoked by the IEP GUI. For potential future extension, all the AFC

experiments already implemented for acoustical stimulation in [27]

can be used for direct electrode stimulation via RIB II. Figure 2 (b)

shows a schematic diagram of the IEP clinical research system’s

software. The GUI offers a user-friendly way to enter patient in-

formation, for parameter selection (e.g. reference CI and electrode),

and for starting the test modules.

In the following system evaluation, the reference CI was left and

the reference electrode was electrode number 5, referred to as L5.

Eight electrodes in the contralateral CI (right) were selected (R1-

R6, R9, R12). There were thus 8 electrode pairs, namely [L5, R1],

[L5, R2], [L5, R3], [L5, R4], [L5, R5], [L5, R6], [L5, R9], [L5,

R12]. The stimulus was a train of charge-balanced biphasic pulses,

with 60 µs phase duration, and 2.1 µs interphase gap presented via

monopolar stimulation mode. All stimuli for these experiments were

constant amplitude pulse trains presented at a rate of 19.9 pulses per

second (pps), either to a single electrode or to an interaural pair of

electrodes. The rate of pulsatile stimulation was lower than typical

stimulation rates used in clinical CI processors but optimal for the

assessment of BIC [13]. Moreover, IPTD perception is improved at

low stimulation rates [28]. The participants’ responses during the

psychophysical testing were obtained using a touch screen monitor

connected to the stimulation computer. For psychophysical testing,

400-ms pulse trains (i.e. a train of 8 pulses) were used, while for

EEG, the electrical pulse train was presented continuously.

67

3.2. Psychophysical tests

Tests are performed in the following order: Loudness estimates ob-

tain the participant’s dynamic range (DR) by measuring the maxi-

mum comfortable level and the hearing threshold. The loudness bal-

ancing procedure is performed for each interaural electrode pair. The

stimulation levels judged by the participants to be equally loud are

saved and used in the pitch ranking and BIC recording procedures,

respectively. The sound image centering is a pre-testing procedure

for IPTD sensitivity testing, in which the participants are instruct-

ed to adjust the presented level at one ear to perceive a centralized

sound image. The IPTD sensitivity experiment includes two steps:

the individual IPTD threshold estimation in one electrode pair for

each participant, and the IPTD sensitivity experiment with the esti-

mated individual IPTD threshold for all the selected electrode pairs.

Each participant receives detailed written instructions before each

specific experiment. The participant then responds to stimulation by

pressing different buttons on the touch screen as instructed for the

specific procedures.

3.2.1. Loudness estimation

Each reference electrode is stimulated individually, and a simple

loudness adjustment procedure employing a touch screen is used to

determine the MCL and HL. In the MCL testing, the stimulation lev-

el is set initially to each CI participant’s clinical comfortable level.

The participants were instructed to respond via the touch screen on

the experiment GUI by pressing ‘increase’ or ‘decrease’ buttons to

change the present sound levels, and to press the ‘OK’ button when

the stimulus was ‘very loud but still comfortable’. A factor of 1.2

is initially used to multiply (for increase) or to divide the stimula-

tion current for adjustment and reduced to 1.05 after the first change

of direction during the adjustment. The final presentation level is

then stored as MCL. Once the MCL is determined, the participant

is asked to adjust the stimulation level to be ‘just audible’ following

the same procedure. The resulting level is then saved as HL. This

MCL and HL procedure is repeated three times for each electrode.

The dynamic range to current unit mapping is then calculated from

the median MCL and HL.

3.2.2. Loudness balance

Interaurally loudness-balanced levels for each electrode pair (i.e. 8

pairs) are determined by an analogous adjustment procedure to that

used for loudness estimation. The members of each electrode pair

are stimulated in two successive intervals in random order. The s-

timulus presented to the reference CI electrode is fixed in level (60%

of DR). The same pulse train stimulus is then presented to one of the

test CI electrodes contralaterally (e.g. R3). The participant then in-

dicates which of the two stimulus bursts was louder. The procedure

adjusts the level with a factor of 1.2, which is then reduced to 1.05

after the first reversal of adjustment direction. The participant termi-

nates the procedure by pressing the ‘OK’ button once the stimuli in

both ears are perceived as equally loud. The number of repetitions

of the measurement for each electrode pair can be adjusted and the

average across repetitions is then calculated as final result.

3.2.3. Interaural pitch ranking

Members of each interaural electrode pair are directly compared for

perceived pitch, using a constant stimulus procedure. Each of these

electrode pair members are stimulated in a random order. The par-

ticipants are asked to indicate in which interval the higher pitch is

perceived. The participants are instructed to focus on pitch rather

than timbre or loudness.

Here, a selected reference electrode (L5) was paired with 8 tar-

get electrodes and each pair was presented ten times, yielding 80

judgments. This experiment was repeated 5 times per reference elec-

trode, yielding 50 responses per electrode pair. Electrode pairs with

an average discriminability across 50 repetitions within the range of

chance (50 ± 14%, corresponding to the 95% confidence interval)

were considered as pitch-matched. For participants with more than

one pitch-matched electrode pair, the pair at the medial tonotopic po-

sition was chosen. The results of all 8 electrode pairs were calculated

and stored.

3.2.4. Sound image centering

A lateralization task is performed on each electrode pair to ensure

that a single, fused auditory image is perceived in the center of the

head. The members of each electrode pair are stimulated simultane-

ously with zero IPTD.

Here, the reference electrode (L5) had a fixed level (60% of

DR) and the presentation level of the contralateral target electrode

was adjusted in level according to the participant’s response. After

each bilateral stimulation (one interval) the participant selected one

of four response alternatives (‘left of the center’, ‘right of the center’,

‘exactly from the center’, or ‘other’) according to their perception

of the sound image. The ‘other’ button was used in the following

cases: more than one sound source was perceived; there was only

one sound image, but it could not be adjusted to be centralized after

considerable time; the sound could not be fused [15]. Only those

electrode pairs for which the participants terminated the experimen-

t with responding ‘exactly from the center’ are selected for further

IPTD sensitivity testing in the next experimental procedure.

3.2.5. IPTD sensitivity testing

The goal of this procedure is to systematically investigate the effects

of interaural electrode pairing on IPTD discrimination. The member-

s of each electrode pair that yield a centralized fused sound image in

the previous experiment are stimulated simultaneously with the pre-

sentation level on the reference electrode (L5) at a fixed level (60%

of DR) and the presentation level of the electrodes on the other ear

resulting from the sound image centering. A series of measurements

using the constant stimulus procedure is used.

Here, each presentation consisted of two 500-ms intervals sepa-

rated by a 300-ms pause. For a fixed IPTD, in one randomly selected

interval a left-leading IPTD of IPTD/2 was introduced while the oth-

er interval carried a right-leading IPTD of IPTD/2. The participant

was required to indicate whether the stimulus in the second interval

was perceived from a lateral position either to the left or the right of

the first interval.

First, an IPTD of 700 µs was chosen and 20 two-interval trials

were presented for the electrode pair, i.e. [L5, R5]. If the correctly

identified lateral positions were between 65 to 85%, the IPTD was

defined as threshold IPTD. If the correct rate was lower or higher, the

IPTD was increased or decreased respectively and the experiment

was repeated until a threshold IPTD was found.

The final IPTD sensitivity experiment was performed using the

above determined threshold IPTD and the same procedure for all

electrode pairs under investigation, i.e. 8 pairs here. The thresh-

old IPTD from the pre-test ensures performance well above chance

but below ceiling performance, independent of the participant’s in-

dividual sensitivity. Each electrode pair was stimulated ten times in

68

60

80

100orr

ect

rate

(%

)

1 2 3 4 5 6 9 120

20

40

Matched electrode number (Right ear)

Perc

enta

ge c

or

IPTD

Pitch ranking

Fig. 3. Results of pitch ranking and IPTD sensitivity procedures for

the 8 selected electrode pairs. The electrode pairs within the range of

the chance level (50± 14%, dashed lines) were considered as pitch-

matched, in this case [L5, R5]. IPTD performance was best for [L5,

R4] and [L5, R5].

a random order. The experiment was repeated 5 times, yielding 50

repetitions for each electrode pair. The correct rate was determined

for all 8 electrode pairs.

3.3. EEG recording and analysis

EEG is differentially recorded from Ag/AgCl electrodes of the in-

ternational 10-20 system [29]. In the data shown here, a single

Ag/AgCl electrode at A1 was recorded, with an electrode at FPz

serving as the ground, and Cz as the physical reference. The partic-

ipant was seated in a recliner and watched a silent subtitled movie

within an electrically shielded sound-attenuating booth. EEG is pre-

amplified with a gain of 150 by a headbox and, in turn, amplified in

a DC-coupled manner with a gain of 5000. An analog second-order

lowpass with a 3-kHz corner frequency is applied by the DSP card

of a Synamps 5083 (Neuroscan, Hampstead, New Hampshire, US-

A), and the signal is digitized at 50 kHz to 16-bit resolution by the

A/D convertor of the Synamps system. EABRs evoked by monau-

ral and bilateral stimulation are derived by epoching the EEG from

-25 to 30 ms post-stimulus onset online. Epochs are averaged online

for each bilateral interaural electrode pair separately and for each

monaural electrode separately, and these separate averages are then

corrected offline such that EABR amplitudes are relative to a 1.000

ms prestimulus baseline prior to the CI artifact that is caused by the

biphasic CI pulse. Electrically evoked BICs are then derived offline.

4. EVALUATION OF THE IEP SYSTEM

The IEP clinical research system was evaluated with two cochlear

implantees with postlingual onset of bilateral severe-to-profound

sensorineural hearing loss and MED-EL implant systems. Voluntary

informed written consent was obtained with the approval of the

Ethics Committee of the University of Oldenburg.

The results of pitch ranking and IPTD sensitivity procedures for

the 8 selected electrode pairs of 1 subject’s are depicted in Fig. 3

as a function of the electrode number. For the pitch ranking, val-

ues below the chance level indicate a lower pitch at the test electrode

compared to the reference electrode, while values above chance level

indicate a higher pitch percept at the test electrode side. The elec-

trode pairs within the range of the chance level (50±14 %, indicated

0 2 4 6 8 10

x 10-3

0

1

2

3

4

Time (ms)

Am

plit

ud

e

L

R

B

BIC

1 V

Fig. 4. EABRs and the BIC results for one exemplary electrode

pair: EABRs of left CI stimulated only, right CI stimulated only,

both CI stimulated simultaneously and the BIC. The y-axis is their

amplitude values in µV, with additive offsets of 4, 2, 1.5 and 0.1 µV

respectively. The electric artifact can be seen at 0 ms, while wave eIII

and eV are visible at approximately 1.7 and 3.3 ms, respectively.

by the dashed horizontal lines) were considered as pitch-matched,

for this case [L5, R5]. The IPTD performance is indicated by the

black squares and was highest for the two electrode pairs [L5, R4]

and [L5, R5]. High performance in the IPTD task coincided with

pitch matching.

The left and right monaural EABRs, the bilateral EABR and the

BIC for one electrode pair, [L5, R3], are shown in Fig. 4. For illus-

tration purpose, vertical offsets of 4, 2, 1.5, and 0.1 µV were added

to the four traces from top to bottom, respectively. The BIC response

consisted of a negative peak at 3.3 ms followed by a positive peak

around 4 ms, as commensurate with the literature [13, 16].

5. SUMMARY AND CONCLUSIONS

The typically observed large variability of performance in Binaural

CIs is partially attributable to a mismatch in the place-of-stimulation

arising from electrode arrays being inserted at different depths in

each cochlea. Here, a clinical research system for interaural elec-

trode pairing (IEP) in BiCIs is designed and evaluated. A user-

friendly GUI for the IEP experiment system controls an existing psy-

chophysical measurement system (AFC [27]) embedded in the IEP

system which was enhanced by an interface module to the MED-EL

RIB II. The IEP experiment system includes several state-of-the-art

psychophysical IEP methods, including pitch ranking, IPTD sensi-

tivity and a binaural and monaural EABR recording module for BIC

measurements.

Evaluation with two adult bilateral CI participants demonstrated

the system’s functionality and plausible results for the psychophysi-

cal IEP methods and a clear BIC were obtained. In the future, more

implantees will be recruited and tested with the IEP system. Results

of the different electrode pairing methods will be compared to find

relations between different pairing methods and for developing an

improved interaural electrode pairing strategy for BiCI users. The

refined IEP clinical research system is planned to be made available

for research and non-commercial applications.

69

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